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Estrogen Receptor-␤ Expression in Human Testicular Germ Cell Tumors

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Estrogen Receptor-␤ Expression in Human Testicular Germ Cell Tumors Vol. 9, 4475–4482, October 1, 2003 Clinical Cancer Research 4475 Estrogen Receptor-␤ Expression in Human Testicular Germ Cell Tumors Vernon Pais,1 Irwin Leav, Kin-Mang Lau,2 gene, was localized to spermatagonia of the normal testis, Zhong Jiang, and Shuk-Mei Ho3 but its expression dramatically reduced in seminomas. With the exception of spermatagonia, androgen receptor was Division of Urology, Department of Surgery [V. P., K-M. L., S-M. H.], and Departments of Pathology [I. L., Z. J.], Cell Biology found in all of the germ cells of the normal testis, but, aside [S-M. H.], and Physiology [S-M. H.], University of Massachusetts from trace staining in 3 of 5 endodermal sinus tumor cells, Medical School, Worcester, Massachusetts 01605, and Department of it was not detected immunohistochemically in any other Pathology, Tufts University School of Veterinary Medicine, Grafton, germ cell cancer. Massachusetts [I. L.] Conclusions: We confirm expression of ER-␤, but not ER-␣, in normal testicular cells, suggesting that only the ABSTRACT former ER subtype mediates the action of estrogen in the Purpose: Estrogen exposure has been linked to a risk human male gonad. Our results provide the first evidence ␤ for the development of testicular germ cell cancers. The that only ER- is expressed in testicular germ cell tumors. effects of estrogen are now known to be mediated by estro- Its expression is down-regulated in seminomas and embry- gen receptor (ER)-␣ and -␤ receptor subtypes, but only onal cell carcinomas but remains high in endodermal sinus ␤ ER-␤ has been found in human normal testis. The goal of tumors and in teratomas. The observed differences in ER- the present study was to compare the localization and ex- expression levels among different testicular germ cell pression levels of these ER subtypes in testicular germ cell tumors may reflect divergent pathways of differentiation/ cancers (seminomas and nonseminomatous germ cell tu- dedifferentiation of these neoplasms from a common mors) with normal testis. For completeness, expression of precursor. Collectively, these findings provide a possible androgen and progesterone receptors was also investigated. mechanistic link between estrogen exposure and testicular Experimental Design: Immunohistochemistry was used cancer risk. to localize the expression of steroid receptors in 39 archival testicular germ cell cancers and 5 morphologically normal INTRODUCTION testes. Expression of the steroid receptors at the transcript Testicular germ cell tumors are the most common malig- level was semiquantified by reverse transcription-PCR in nancy in males between 15 and 34 years of age, and represent a 5 paired fresh-frozen specimens of normal and neoplastic major cause of death attributable to cancer in this age group (1). testes. Every year, ϳ7400 new cases of testicular tumors are diagnosed Results: ER-␣ was not expressed in the human normal in the United States. The incidence of this type of cancer has testis. It was also absent in all of the testicular germ cell increased progressively throughout the twentieth century (2). cancers studied. In contrast, ER-␤ was strongly expressed in Germ cell tumors can be subdivided into seminoma and various germ cells of the normal testis. However, its expres- NSGCTs,4 which consist of embryonal cell carcinoma, chorio- sion was markedly diminished in seminomas, embryonal cell carcinoma, yolk sac tumor, and teratoma. Neoplasms that con- carcinomas, and in mixed germ cell tumors, at both tran- tain more than one tumor cell components, e.g. seminoma and scriptional and translational levels. In contrast, ER-␤ re- embryonal cell carcinoma, are referred to as mixed germ cell mained highly expressed in endodermal sinus tumors and tumors. Seminoma and NSGCTs not only present with distinc- teratomas. Progesterone receptor, an estrogen-regulated tive clinical features, they also differ with respect to therapy and prognosis (3). Whereas the etiology of testicular germ cell cancers re- mains undefined, exposure to certain hormones (in particular estrogen) at the time of testicular differentiation in utero has Received 12/31/02; revised 5/16/03; accepted 5/28/03. The costs of publication of this article were defrayed in part by the long been implicated as a risk factor for developing these payment of page charges. This article must therefore be hereby marked neoplasms (4). An earlier case-control study (5) demonstrated advertisement in accordance with 18 U.S.C. Section 1734 solely to first trimester exposure of the mother to exogenous estrogen indicate this fact. produced a 8-fold rise in risk for testicular cancer in the son. This work was supported in part by NIH Grants CA15776 and DK610840, and a United States Army Prostate Cancer Program Grant More recently, other investigations (6, 7) confirmed increased DAMD17-98-1-8606 (to S-M. H.). 1 Present address: Department of Urology, St. Elizabeth’s Medical Cen- ter of Boston, Boston, MA 02135. 2 Present address: Department of Anatomical and Cellular Pathology, Prince of Wales Hospital, Shatin, New Territories, Hong Kong, China. 4 The abbreviations used are: NSGCT, nonseminomatous germ cell 3 To whom requests for reprints should be addressed, at Room S4-746, tumor; ER, estrogen receptor; PR, progesterone receptor; AR, androgen Department of Surgery, University of Massachusetts Medical School, 55 receptor; RT-PCR, reverse transcription-PCR; GAPDH, glyceralde- Lake Avenue North, Worcester, MA 01655. Phone: (508) 856-1909; hyde-3-phosphate dehydrogenase; IGCNU, intratubular germ cell neo- Fax: (508) 856-8699; E-mail: [email protected]. plasia of unclassified type. Downloaded from clincancerres.aacrjournals.org on September 27, 2021. © 2003 American Association for Cancer Research. 4476 Estrogen Receptor-␤ in Testicular Germ Cell Cancer incidences of testicular germ cell tumors in men with maternal logical studies, conducted to localize ER in testicular tumors, exposure to diethylstilbestrol. Furthermore, a higher incidence used only antibodies directed against the ␣ subtype (28). of testicular cancer was observed among men exposed prena- In the current investigation we compared the expression tally to excess maternal hormone as in the case of preterm birth, ER-␤, ER-␣, AR and PR in 39 human testicular germ cell being a twin, and first births among young mothers (6, 8). In malignancies with that found in normal testicular specimens. contrast, a protective effect was noted with in utero exposure to ER-␤ expression was studied at the immunohistochemical level presumed low-estrogen states, such as those associated with using a well-characterized, ER subtype-specific antibody, di- heavy cigarette use and bleeding/threatened miscarriage (6). rected against the F domain of the human receptor (29). Fur- Adult exposure to excess estrogen as in conditions associated thermore, expression of these receptors was studied at the tran- with development of gynecomastia (9), treatment of prostate script level in 5 testicular germ cell cancers and results cancer with estrogen (10), or occupational contact with estrogen compared with expression levels in morphologically normal mimics (e.g. organochlorines; Refs. 11, 12) have all been linked testicular tissues. to a higher risk for testicular cancers. Experimentally, prenatal and postnatal administration of estrogens consistently causes testicular tumor development in some strains of rodents (13). MATERIALS AND METHODS Despite the above-cited epidemiological reports linking Testicular Tissues. Thirty-nine archival cases from rad- estrogens to testicular cancer the mechanisms by which estro- ical orchiectomies and 5 from simple orchiectomies (ages 21– gens contribute to the pathogenesis of these neoplasms remains 57) were selected from the surgical pathology files of the University of Massachusetts Medical School. These specimens unclear. It has been reported that serum estrogen levels are were collected during a 6-month period (at the end of 2000 and elevated in patients with testicular germ-cell cancers (14, 15), a the beginning of 2001). The collection included 17 seminomas, condition which likely resulted from local production by the and 22 NSGCTs consisting of 10 mixed germ cell tumors with tumor tissue, because aromatase activity has been demonstrated embryonal cell components, 5 with endodermal sinus compo- in Leydig cells, Sertoli cells, and various germ cells of the nents, 3 cases of embryonal carcinoma, and 4 cases of mature normal testis (16, 17). A recent report suggests that the carci- teratomas. Serial sections, 5–6 ␮m, were cut from paraffin- nogenic effects of estrogen on testicular cells may involve embedded specimens, mounted on glass slides, and stored un- ER-mediated oxidative DNA damage (18). In this study, expo- baked until immunohistochemistry was performed. ␣ sure of rat testicular cells to 17 -ethinylestradiol caused in- In addition, transcript expression was studied with mRNA Ј creased formation of 7, 8-dihydro-8-oxo-2 -dexoyguanosine, a extracted from 5 simple orchiectomy surgical specimens and marker of oxidative DNA-damage, which could be blocked by compared those in extracts from morphologically “normal” tes- cotreatment with a pure ER antagonist. ticular tissues from the ipsilateral testis. On the basis of gross It is now well known that the action of an estrogen on appearance, tumor and “normal” tissues were separately dis- target cells is mediated by its interaction and subsequent acti- sected, and each piece was divided. One half of each sample was vation
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